Circadian Locomotor Activity in Freshwater Decapods: an Ecological Approach

Biological Rhythm Research 2004, Vol. 35 Nos 1/2. pp. 69–78 Circadian Locomotor Activity in Freshwater Decapods: An Ecological Approach Manuel Miranda-Anaya Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, DF 04510, México Abstract Circadian rhythms of locomotor activity shown by freshwater decapods display different patterns among crayfish, Procambarus, and crabs, when exposed to artificial light-dark cycles. Crayfish are mainly nocturnal while a crepuscular activity is observed in crabs of the genus Pseudothelphusa. In constant darkness, free running rhythms are displayed in unimodal or bimodal patterns by crayfish Procambarus; however, Pseudothelphusa continues to show bimodal rhythms. The many studies using locomotor activity indicate that the rhythm in freshwater crabs is circadian in nature, but that a multioscillatory system may be controlling the overt rhythm. In the present study, the implications of different locomotor activity patterns are analyzed in selected freshwater decapods with regard to the interactions between light and the organisms. Crabs and crayfish are commonly found in similar habitats, often sharing the same environment; however, different patterns of locomotor activity as well as different sensitivities of the bouts of activity with regard to entrainment by light, indicate that distinct temporal niches may exist that result in temporal exclusion or low competition. Keywords: Freshwater crab, circadian rhythm, locomotor activity. Introduction Ecological studies on biological timing in organisms allows an understanding of the temporal relationship of behavior and geophysical changes; therefore it is possible to study the mechanisms underlying the interactions of organisms and their environment by studying their clock output. Decapods are a diverse group found in a wide diver- sity of habitats, from deep sea to fresh water and land. Their ability to adapt to diverse Address correspondence to: Dr. Manuel Miranda-Anaya, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, México DF 04510, México. E-mail: mma@ hp.fciencias.unam.mx DOI: 10.1080/09291010412331313241 © 2004 Taylor & Francis Ltd. 70 M. Miranda-Anaya conditions generates many questions about physiological adaptations that allow this group to be successful. Many studies on circadian organization in crustaceans have used locomotor activity as a measure of the output of the clock, and most of the observations have been in performed in laboratory, presumably because of difficulties in long-term observation in natural aquatic habitats (DeCoursey, 1983). Decapods have, for several years, been a biological model for studying circadian organization in Crustacea (Warner, 1977; DeCoursey, 1983; Brown, 1983; Aréchiga et al., 1993; Fuentes-Pardo & Hernández-Falcón, 1993). The crayfish, Procambarus, has been extensively studied, since it displays circadian rhythms in physiological fea- tures; locomotor activity, in particular, has been widely studied (Page & Larimer, 1972, 1975; Fanjul-Moles, 1998; Fuentes-Pardo et al., 1996). Studies on circadian rhythms of activity in freshwater decapods have shown that activity patterns may be different among crayfishes and crabs sharing similar habitats. The freshwater crab, Pseudothelphusa, is often found in habitats where other crayfish species coexist (Álvarez & Villalobos, 1997; López-Hernández, 1997). Studying differences in their circadian activity under laboratory conditions may be useful in understanding the temporal relationship between each species regarding the physical and biological rhythmic environment where they are found. In this paper, we present a summary of the circadian characteristics of locomotor activity displayed by species of Procambarus and the freshwater crab, Pseudothelphusa, as well as an interpretation of the ecological significance of these locomotor activity patterns. I. Freshwater decapods and the environment Freshwater decapods are found in habitats such as standing water (for example, lakes and ponds — lentic) and flowing water (for example, streams and rivers — lotic). Each of these habitats presents a varied set of environmental characteristics. The most obvious factor in freshwater environments is the low salinity and the complex inter- action of this with other factors such as temperature. Other differences associated with the temporary and isolated nature of freshwater ponds and streams may limit the distribution of crustaceans (Vernberg & Vernberg, 1983). Freshwater decapods are represented by crayfish of the family Cambaridae, Astacidae and Parastacidae (Hobbs et al., 1989) and by crabs of the family Pseudothelphusidae and Trichodactilidae (Álvarez & Villalobos, 1997). There is little information about the biology of freshwater Brachyurans (true crabs); however, extensive information about of crayfish biology has been documented elsewhere (Hobbs, 1988; Holdich, 2002). Crayfish and crabs are frequent in slow streams of clean water and near the river shore, living in places where they can hide, like in flooded roots or under stones. Crayfish dig tunnels in soft soil and can remain inside for long periods of time. Field observations of locomotor activity of crayfish indicate that adults are mainly nocturnal, but activity may begin in the late afternoon. Most of the species of freshwater decapods present small populations, high morphologic differentiation within the population, and reduced distribution areas (Álvarez & Villalobos, 1997). It is common to find both crayfish and crabs in lakes Circadian Rhythms of Activity in Freshwater Decapods 71 and rivers from Southern Mexico to tropical South America as a component of the aquatic fauna (López-Hernández, 1997). Both crayfish and crabs are omnivorous and usually feed on plants and small animals. II. Laboratory studies on locomotor activity in freshwater decapods Freely moving locomotor activity rhythms in freshwater decapods have often been analyzed by means of tilt cages (Page & Larimer, 1972) or of aquaria equipped with infrared light-crossings (Fanjul-Moles et al., 1996; Miranda-Anaya et al., 2003a). Locomotor activity has been also recorded from restrained animals, with a thread tied to the ambulatory legs and movement recorded by a force transducer (Fuentes-Pardo & Inclán-Rubio, 1981; Viccon-Pale & Fuentes-Pardo, 1994). Locomotor activity in decapods is often mathematically ‘noisy’; however, some statistical tools have been used to analyze significant circadian behavior (DeCoursey, 1983). Methods used include plotting data in conventional actograms, and calculating circadian periods by means of Enright’s and the X2 periodograms (Enright, 1965; Sokolove & Bushell, 1978). In species like Procambarus clarkii, circadian rhythms of locomotor activity manifest themselves gradually after the first week post hatching, and this has allowed study of the ontogenetic expression of locomotor activity rhythms (Fanjul-Moles et al., 1996; Miranda-Anaya & Fanjul-Moles, 1997). Studies of circadian locomotor activity rhythms in crustaceans have been performed not only in Procambarus clarkii but also in other crayfish species like P bouvierii (Fuentes-Pardo & Inclán-Rubio, 1981) and P. diguetti (Fanjul-Moles et al., 1998b). Both freely moving and restrained animals kept in LD cycles display mainly two peaks of activity, an induced short burst right after lights on and an endogenous long burst after lights off, typical for a nocturnal animal (Page & Larimer, 1972). When placed in constant darkness (DD), their locomotor activity displays mainly a unimodal pattern (Page & Larimer, 1972; Fanjul-Moles, 1998); however, bimodal patterns have been observed in some studies (Fuentes-Pardo et al., 1996). Figure 1 represents a typical actogram obtained from an adult crayfish in freely moving conditions using infrared light crossings. In constant darkness (DD) locomotor activity is usually noisy during the first days of recording; however, circadian rhythms are seen after about four days in DD. Activity becomes bimodal with multi- ple short bouts. The circadian rhythm of locomotion in crayfish has been considered as unimodal (Page & Larimer, 1972; Fanjul-Moles et al., 1996) but sometimes it is possible to observe bimodal activity with alternate dominance of each bout (Fuentes- Pardo & Inclán-Rubio, 1981; Gherardhi, 2002; and Fig. 1). During LD, a short bout of activity is observed at lights on, and a larger bout of activity which starts before lights off and continues until well after lights off. The cor- responding waveform (upper right) shows the average activity during DD, there being a clear indication of its bimodal nature. Entraining locomotor activity of the crayfish to an LD cycle denotes typical nocturnal behavior, again with bimodal rhythmicity (lower right). The waveform derived from 9 consecutive days shows that activity peaks are coincident with lights on and lights off respectively (arrow). The duration of the two peaks indicates that the lights-off bout represents the main activity episode, and 72 M. Miranda-Anaya DD A 300 150 Activity 0 0 12.6 25.3 LD B 300 YS ty DA 150 Activi 0 0 12 24 Time (h) 24 24 24 TIME OF DAY (h) Figure 1. Double-plot of locomotor activity in a freshwater crayfish Procambarus clarkii. In DD (upper arrow), a circadian rhythm is observed with two bouts of activity, represented in the waveform (A) fitted to the dominant period. In LD (second arrow) an activity peak is coincident with lights on, also observed in the waveform (B). the lights-on

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